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Mycobacterium bovis Infection in Red Foxes in Four Animal Tuberculosis Endemic Areas in France.

ABSTRACT: In France, animal tuberculosis (TB) due to Mycobacterium bovis (M. bovis) affects a multi-host community that include cattle and wildlife species such as wild boars (Sus scrofa), badgers (Meles meles), or wild deer (Cervus elaphus, Capreolus capreolus). The involvement of foxes in the epidemiology of TB is fairly described in countries facing multispecies concerns. After the discovery of grouped cases of TB in foxes in a French TB endemic region, a study was implemented in the core of four TB endemic areas in Dordogne, Charente, Landes (departments of Nouvelle-Aquitaine region), and Côte-d'Or (Burgundy-Franche-Comté region). No infected fox was found in Côte-d'Or (n = 146), where in parallel TB in cattle and other wild species became sparse in the last years. In contrast, in Dordogne, Charente, and Landes, 13 (n = 184), 9 (n = 98) and 7 (n = 140) foxes were found infected by M. bovis, respectively, corresponding to 7.1% (CI95% 3.8-11.8%), 9.2% (4.3-16.7%) and 5.0% (CI95% 2.0-10.0%) prevalence rates, respectively. These infection rates are comparable with those observed in badgers and wild boar in these same three areas (ranging from 9 to 13.2% and 4.3 to 17.9%, respectively), where the number of cattle outbreaks has increased in the last 10-15 years. In each area, the genotypes of foxes' M. bovis isolates were the same as those in local cattle and other wildlife species. None of the infected foxes presented TB-like gross lesions. M. bovis was found in the mesenteric lymph nodes of 28 foxes (68%). For the 12 foxes where retropharyngeal and respiratory lymph nodes were analyzed separately, M. bovis was present in the respiratory lymph nodes of eight individuals. With regard to excretion, appropriate samples were available for 12 infected foxes from Dordogne. M. bovis DNA was detected in the feces of five of these animals, four of which were infected in the mesenteric lymph nodes. Combined with the knowledge on the biology and ecology of foxes, the results of this study suggest that in areas where infection in cattle is still active in France, foxes might play a role of spillover host in the epidemiology of M. bovis.

SUBMITTER: Richomme C

PROVIDER: S-EPMC7409206 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Mycobacterium bovis Infection in Red Foxes in Four Animal Tuberculosis Endemic Areas in France.

Richomme Céline C Réveillaud Edouard E Moyen Jean-Louis JL Sabatier Perrine P De Cruz Krystel K Michelet Lorraine L Boschiroli Maria Laura ML

Microorganisms 20200717 7

In France, animal tuberculosis (TB) due to Mycobacterium bovis (M. bovis) affects a multi-host community that include cattle and wildlife species such as wild boars (Sus scrofa), badgers (Meles meles), or wild deer (Cervus elaphus, Capreolus capreolus). The involvement of foxes in the epidemiology of TB is fairly described in countries facing multispecies concerns. After the discovery of grouped cases of TB in foxes in a French TB endemic region, a study ...[more]

PMID: 32709124

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Project description:In Europe, animal tuberculosis (TB) due to Mycobacterium bovis involves multi-host communities that include cattle and wildlife species, such as wild boar (Sus scrofa), badgers (Meles meles) and red deer (Cervus elaphus). Red fox (Vulpes vulpes) infections have also been recently reported in some TB endemic regions in the Iberian Peninsula and France, with some of the infected animals shedding M. bovis in urine and feces. In order to understand the pathogenesis of M. bovis infection in foxes and the associated risk of transmission, 12 captive foxes (6 females and 6 males) were inoculated orally with 2 × 107 colony-forming units of a French field isolate of M. bovis. Clinical samples (urine, feces and oropharyngeal swabs) were collected every four weeks and tested for molecular diagnosis and bacteriology. Serological responses were measured by IDEXX M. bovis Ab Test and Multi Antigen Print Immunoassay (MAPIA). At a post-mortem examination performed 12 weeks post infection (wpi), tissues were tested for the presence of M. bovis and associated gross and microscopic TB-like lesions. M. bovis was detected by PCR in bladder swabs of 3 animals at 12 wpi. It was also detected pre-mortem at different time points of the experiment in the oropharyngeal mucus of three individuals and in the feces of nine foxes, with two of them confirmed by bacteriology. All 12 foxes had at least 4 PCR positive samples (out of the 23 tested), and all but 1 fox had at least 1 culture positive sample. The culture negative fox was PCR positive in both retropharyngeal and mesenteric lymph nodes, in line with the results of the other animals. Seroconversion was observed in all foxes except one during the experiment, and in nine at the final time point. No gross visible lesions were found in any animal at the post-mortem examination. The histology showed small granulomas within the lymph nodes, tonsils, liver and lungs from eight animals, with the presence of few acid-fast bacilli. These results confirmed that all orally-infected foxes developed mild TB lesions but they were able to shed mycobacteria in about 75% of cases, 1 month post-infection (9 out 12 foxes). These results show that it is possible to induce typical TB infection experimentally in captive foxes, with measurable M. bovis excretion; such an experimental system could be useful for future evaluations of diagnostics and vaccines in this species.

Project description:Mycobacterium bovis causes bovine tuberculosis and is the main organism responsible for zoonotic tuberculosis in humans. We performed the sequencing, assembly and annotation of a Brazilian strain of M. bovis named SP38, and performed comparative genomics of M. bovis genomes deposited in GenBank. M. bovis SP38 has a traditional tuberculous mycobacterium genome of 4,347,648 bp, with 65.5% GC, and 4,216 genes. The majority of CDSs (2,805, 69.3%) have predictive function, while 1,206 (30.07%) are hypothetical. For comparative analysis, 31 M. bovis, 32 M. bovis BCG, and 23 Mycobacterium tuberculosis genomes available in GenBank were selected. M. bovis RDs (regions of difference) and Clonal Complexes (CC) were identified in silico. Genome dynamics of bacterial groups were analyzed by gene orthology and polymorphic sites identification. M. bovis polymorphic sites were used to construct a phylogenetic tree. Our RD analyses resulted in the exclusion of three genomes, mistakenly annotated as virulent M. bovis. M. bovis SP38 along with strain 35 represent the first report of CC European 2 in Brazil, whereas two other M. bovis strains failed to be classified within current CC. Results of M. bovis orthologous genes analysis suggest a process of genome remodeling through genomic decay and gene duplication. Quantification, pairwise comparisons and distribution analyses of polymorphic sites demonstrate greater genetic variability of M. tuberculosis when compared to M. bovis and M. bovis BCG (p ≤ 0.05), indicating that currently defined M. tuberculosis lineages are more genetically diverse than M. bovis CC and animal-adapted MTC (M. tuberculosis Complex) species. As expected, polymorphic sites annotation shows that M. bovis BCG are subjected to different evolutionary pressures when compared to virulent mycobacteria. Lastly, M. bovis phylogeny indicates that polymorphic sites may be used as markers of M. bovis lineages in association with CC. Our findings highlight the need to better understand host-pathogen co-evolution in genetically homogeneous and/or diverse host populations, considering the fact that M. bovis has a broader host range when compared to M. tuberculosis. Also, the identification of M. bovis genomes not classified within CC indicates that the diversity of M. bovis lineages may be larger than previously thought or that current classification should be reviewed.

Dataset Information

Mycobacterium bovis Infection in Red Foxes in Four Animal Tuberculosis Endemic Areas in France.

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<i>Mycobacterium bovis</i> Infection in Red Foxes in Four Animal Tuberculosis Endemic Areas in France.

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